XB-ART-56277PLoS One January 1, 2019; 14 (9): e0222106.
Action spectrum for photoperiodic control of thyroid-stimulating hormone in Japanese quail (Coturnix japonica).
At higher latitudes, vertebrates exhibit a seasonal cycle of reproduction in response to changes in day-length, referred to as photoperiodism. Extended day-length induces thyroid-stimulating hormone in the pars tuberalis of the pituitary gland. This hormone triggers the local activation of thyroid hormone in the mediobasal hypothalamus and eventually induces gonadal development. In avian species, light information associated with day-length is detected through photoreceptors located in deep-brain regions. Within these regions, the expressions of multiple photoreceptive molecules, opsins, have been observed. However, even though the Japanese quail is an excellent model for photoperiodism because of its robust and significant seasonal responses in reproduction, a comprehensive understanding of photoreceptors in the quail brain remains undeveloped. In this study, we initially analyzed an action spectrum using photoperiodically induced expression of the beta subunit genes of thyroid-stimulating hormone in quail. Among seven wavelengths examined, we detected maximum sensitivity of the action spectrum at 500 nm. The low value for goodness of fit in the alignment with a template of retinal1-based photopigment, assuming a spectrum associated with a single opsin, proposed the possible involvement of multiple opsins rather than a single opsin. Analysis of gene expression in the septal region and hypothalamus, regions hypothesized to be photosensitive in quail, revealed mRNA expression of a mammal-like melanopsin in the infundibular nucleus within the mediobasal hypothalamus. However, no significant diurnal changes were observed for genes in the infundibular nucleus. Xenopus-like melanopsin, a further isoform of melanopsin in birds, was detected in neither the septal region nor the infundibular nucleus. These results suggest that the mammal-like melanopsin expressed in the infundibular nucleus within the mediobasal hypothalamus could be candidate deep-brain photoreceptive molecule in Japanese quail. Investigation of the functional involvement of mammal-like melanopsin-expressing cells in photoperiodism will be required for further conclusions.
PubMed ID: 31509560
PMC ID: PMC6738599
Article link: PLoS One
Species referenced: Xenopus laevis
Genes referenced: opn4 ptch1 tshb XB5957215 [provisional]
Article Images: [+] show captions
|Fig 1. Spectral characteristics of the transmittance of various wavelengths of light reaching the quail hypothalamus.Relative transmittance pattern (T/Tmax) of various wavelengths of light penetrating the feathers, skin, skull, and brain tissue are indicated. Each point represents the mean ±SEM (n = 3).|
|Fig 2. The action spectrum using the photoperiodically induced beta subunit of thyroid-stimulating hormone.(A) Schedule for light exposure and sampling. Eye-patched birds lacking pineal organ and maintained under short-day conditions (6 h:18 h light/dark cycle: 6L18D) were given a long-day stimulus by extending the 6-h light period by 10 h with light of seven different wavelengths. (B) The effects of four intensities of light at each wavelength on the expressions of photoperiodically induced mRNA encoding the beta subunit of thyroid-stimulating hormone (TSHB) in the pars tuberalis of the pituitary gland were evaluated by in situ hybridization. (C) Each expression level of TSHB was plotted to examine the dependence of photoperiodic responses on irradiance with monochromatic lights of seven different wavelengths. Each light intensity (photons m2 s-1) was adjusted to the light intensity at the deep-brain region level using the percentage of T/Tmax. Each point represents the mean ± SEM (n = 4). (D) The action spectrum for photoperiodic TSHB induction. The half-saturation constant (EC50) derived from sigmoidal fits of the light intensity–response curves were plotted against wavelength. The action spectrum was then fitted with a curve for retinal1-based photopigment using the least-squares method. Peak sensitivity was approximately 479.2 nm with a low value for the goodness of fit (adjusted R2 = -0.938).|
|Fig 3. Expressions of mammal-like and Xenopus-like melanopsins in the quail brain.(A) The expression of mRNA encoding mammal-like melanopsin (OPN4m) was detected in the infundibular nucleus (IN) within the mediobasal hypothalamus (MBH) (arrowheads in the lower row); however, OPN4m was not detected in the septal region. Faint expression of Xenopus-like melanopsin (OPN4x) mRNA was detected in the septal region (arrowheads in the upper raw) but was not detected in the MBH. (B) Expression analysis of both melanopsins based on high-sensitivity in situ hybridization revealed the expression of OPN4m in the IN (arrowheads in a high-magnification image). (C) The JTK_CYCLE algorithm revealed a pattern of OPN4m expression in the IN that lacked a distinctive periodicity (adjusted p-value: 1.0, Benjamini–Hochberg q-value: 1.0, period: 20, Phase 12). Each point represents the mean ± SEM (n = 3). CO: optic chiasm, IN: infundibular nucleus, LS: lateral septum, LV: lateral ventricle, ME: median eminence, PVO: paraventricular organ, 3V: third ventricle.|
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